Storage of verbal associations is sufficient to activate the left medial temporal lobe

Neuroimaging studies have shown that memory encoding activates the medial temporal lobe (MTL). Many believe that these activations are related to novelty but it remains unproven which is critical - novelty detection or the rich associative encoding it triggers. We examined MTL activation during verbal associative encoding using functional magnetic resonance imaging. First, associative encoding activated left posterior MTL more than single word encoding even though novelty detection was matched, indicating not only that associative encoding activates the MTL particularly strongly, but also that activation does not require novelty detection. Moreover, it remains to be convincingly shown that novelty detection alone does produce such activation. Second, repetitive associative encoding produced less MTL activation than initial associative encoding, indicating that priming of associative information reduces MTL activation. Third, re-encoding familiar associations in a well-established way had a minimal effect on both memory and MTL activation, indicating that MTL activation reflects storage of associations, not merely their initial representation.     

Anterior medial temporal lobe activation during encoding of words: FMRI methods to optimize sensitivity

The existence of a rostrocaudal gradient of medial temporal lobe (MTL) activation during memory encoding has historically received support from positron emission tomography studies, but less so from functional MRI (FMRI) studies. More recently, FMRI studies have demonstrated that characteristics of the stimuli can affect the location of activation seen in the MTL when those stimuli are encoded. The current study tested the hypothesis that MTL activation during memory encoding is related to the modality of stimulus presentation. Subjects encoded auditorily or visually presented words in an FMRI novelty paradigm. Imaging and analysis parameters were optimized to minimize susceptibility artifact in the anterior MTL. Greater activation was observed in the anterior than posterior MTL for both modalities of stimulus presentation. The results indicate that anterior MTL activation occurred during encoding, independent of stimulus modality and provide support for the hypothesis that verbal-semantic memory processing occurs in anterior MTL. The authors suggest that technical factors are critical for observing the rostrocaudal gradient in MTL memory activation.     

Decreased parahippocampal activity in associative priming: evidence from an event-related fMRI study

In recent years, there has been intense debate on the neural basis of associative priming, particularly on the role of the medial temporal lobe (MTL) in retrieving associative information without awareness. In this study, event-related fMRI was used while healthy subjects performed a perceptual identification task on briefly presented unrelated word pairs and an associative recognition memory task. Contamination of priming by explicit memory was successfully controlled, as associative priming and explicit memory were dissociated on the behavioral level. The fMRI results showed a functional dissociation within the MTL with respect to associative priming effects. The right parahippocampal cortex, but not the hippocampus, showed decreased activation for old vs. new pairs and old vs. recombined pairs (associative priming). The bilateral hippocampus and the right parahippocampal cortex were involved in explicit associative memory. These data provide evidence that subregions of the MTL participate in associative priming even when explicit involvement was controlled. Thus, different regions within the MTL play distinct roles in explicit and implicit associative memory.     

Disproportionate deficit in associative recognition relative to item recognition in global amnesia

In two experiments, we tested the hypothesis that medial temporal lobe (MTL) amnesic patients and, likewise, diencephalic (DNC) amnesic patients evidence a disproportionate deficit in memory for associations in comparison with memory for single items. In Experiment 1, we equated item recognition in amnesic and control participants and found that, under these conditions, associative recognition remained impaired both for MTL patients and for DNC patients. To rule out an alternative interpretation of the results of Experiment 1, in Experiment 2 we compared the performance of amnesic and control participants on a one-item recognition task and a two-item recognition task that required no memory for the association between members of word pairs. In the MTL group, when single-item recognition was equated to that of the controls, two-item nonassociative pair memory was equivalent as well. In the DNC group, nonassociative pair memory was impaired, but this impairment did not fully account for the impairment in associative memory. These findings indicate that memory for novel associations between items is disproportionately impaired in comparison with memory for single items in amnesia.     

The Neuroimaging of Long-term Memory Encoding Processes

There needs to be more crosstalk between the lesion and functional neuroimaging memory literatures. This is illustrated by a discussion of episode and fact encoding. The lesion literature suggests several hypotheses about which brain regions underlie the storage of episode and fact information, which can be explored by functional neuroimaging. These hypotheses have been underexplored because neuroimaging studies of encoding have been insufficiently hypothesis-driven and have not controlled encoding-related processes sufficiently well to allow clear interpretations of results to be made. Nevertheless, there is good evidence that certain kinds of associative encoding and/or consolidation are sufficient to activate the medial temporal lobes, and preliminary evidence that some kinds of associative priming may reduce activation of this region. It remains to be proved that attentional orienting to certain kinds of novel information activates the medial temporal lobes. Evidence is growing that the HERA model, developed from neuroimaging rather than lesion data, requires modification and that frontal cortex encoding activations are probably caused by executive processes that are important in effortful memory processing. Neuroimaging studies allow the detection of encoding-related activations in previously unexpected brain regions (e.g. parietal lobes) and, in turn, these findings can be explored with lesion studies.     

The neuroimaging of long-term memory encoding processes

There needs to be more crosstalk between the lesion and functional neuroimaging memory literatures. This is illustrated by a discussion of episode and fact encoding. The lesion literature suggests several hypotheses about which brain regions underlie the storage of episode and fact information, which can be explored by functional neuroimaging. These hypotheses have been underexplored because neuroimaging studies of encoding have been insufficiently hypothesis-driven and have not controlled encoding-related processes sufficiently well to allow clear interpretations of results to be made. Nevertheless, there is good evidence that certain kinds of associative encoding and/or consolidation are sufficient to activate the medial temporal lobes, and preliminary evidence that some kinds of associative priming may reduce activation of this region. It remains to be proved that attentional orienting to certain kinds of novel information activates the medial temporal lobes. Evidence is growing that the HERA model, developed from neuroimaging rather than lesion data, requires modification and that frontal cortex encoding activations are probably caused by executive processes that are important in effortful memory processing. Neuroimaging studies allow the detection of encoding-related activations in previously unexpected brain regions (e.g. parietal lobes) and, in turn, these findings can be explored with lesion studies.     

Differential effects of age on item and associative measures of memory: a meta-analysis

In this meta-analysis, the authors evaluated recent suggestions that older adults' episodic memory impairments are partially due to a reduced ability to encode and retrieve associated/bound units of information. Results of 90 studies of episodic memory for both item and associative information in 3,197 young and 3,192 older adults provided support for the age-related associative/binding deficit suggestion, indicating a larger effect of age on memory for associative information than for item information. Moderators assessed included the type of associations, encoding instructions, materials, and test format. Results indicated an age-related associative deficit in memory for source, context, temporal order, spatial location, and item pairings, in both verbal and nonverbal material. An age-related associative deficit was quite pronounced under intentional learning instructions but was not clearly evident under incidental learning instructions. Finally, test format was also found to moderate the associative deficit, with older adults showing an associative/binding deficit when item memory was evaluated via recognition tests but not when item memory was evaluated via recall tests, in which case the age-related deficits were similar for item and associative information.     

The relevance of the nature of learned associations for the differentiation of human memory systems

In a previous functional magnetic resonance imaging (fMRI) study we demonstrated an involvement of the medial temporal lobe (MTL) during an implicit learning task. We concluded that the MTL was engaged because of the complex contingencies that were implicitly learned. In addition, the basal ganglia demonstrated effects of a paralleled proceduralization of fixed stimulus-response associations. In the present study we directly tested the hypothesis that the MTL activation depends upon implementing the complex regularity in task material, whereas activation of basal ganglia does not. Therefore, we rearranged task material such that it did not contain any complex regularity. The statistical comparison of behavioral and fMRI data between the materials allowed for isolating effects that were directly related to the implicit learning process regarding the complex regularity. The results showed a reliable difference of fMRI signal limited to the MTL, indicating a specific functional role of the MTL in implicit learning of complex contingencies. Furthermore, no difference of BOLD (Blood-Oxygenation Level Dependent) signal in the basal ganglia and cerebellum were detected, supporting the assumption of a functional involvement of the structures in proceduralization of simple stimulus-response associations but not in implicitly learning complex relations. We therefore conclude that the nature of the learned associations is relevant for determining the neuronal focus of learning, rather than the accompanying awareness.     

Content-specific source encoding in the human medial temporal lobe

Although the medial temporal lobe (MTL) is known to be essential for episodic encoding, the contributions of individual MTL subregions remain unclear. Data from recognition memory studies have provided evidence that the hippocampus supports relational encoding important for later episodic recollection, whereas the perirhinal cortex has been linked with encoding that supports later item familiarity. However, extant data also strongly implicate the perirhinal cortex in object processing and encoding, suggesting that perirhinal processes may contribute to later episodic recollection of object source details. To investigate this possibility, encoding activation in MTL subregions was analyzed on the basis of subsequent memory outcome while participants processed novel scenes paired with 1 of 6 repeating objects. Specifically, encoding activation correlating with later successful scene recognition memory was evaluated against that of source recollection for the object paired with the scene during encoding. In contrast to studies reporting a link between perirhinal cortex and item familiarity, it was found that encoding activation in the right perirhinal cortex correlates with successful recollection of the paired object. Furthermore, other MTL subregions also exhibited content-specific source encoding patterns of activation, suggesting that MTL subsequent memory effects are sensitive to stimulus category.     

The role of medial temporal lobe in item recognition and source recollection of emotional stimuli

Recent neuroimaging results suggest that distinct regions within the medial temporal lobe (MTL) may differentially support the episodic encoding of item and relational information for nonemotional stimuli (for a review, see Davachi, 2006). The present study was designed to assess whether these findings generalize to emotional stimuli. Behaviorally, we found that emotion reduced item recognition accuracy but did not reliably affect relational memory. fMRI analyses revealed that neutral and emotional words elicited distinct activation patterns within MTL regions predictive of subsequent memory. Consistent with previous findings for neutral words, hippocampal activation predicted later relational memory, whereas activation in the perirhinal cortex predicted successful item recognition. However, for emotional words, activation in the amygdala, hippocampus, and posterior parahippocampal cortex predicted item recognition only. These data suggest that MTL regions differentially support encoding of neutral and emotional stimuli.     

Adult age differences in memory for name-face associations: The effects of intentional and incidental learning

Previous studies have indicated that older adults have a special deficit in the encoding and retrieval of associations. The current study assessed this deficit using ecologically valid name-face pairs. In two experiments, younger and older participants learned a series of name-face pairs under intentional and incidental learning instructions, respectively, and were then tested for their recognition of the faces, the names, and the associations between the names and faces. Under incidental encoding conditions older adults' performance was uniformly lower than younger adults in all three tests, indicating age-related impairments in episodic memory representations. An age-related deficit specific to associations was found under intentional but not under incidental learning conditions, highlighting the importance of strategic associative processes and their decline in older adults. Separate analyses of hits and false alarms indicate that older adults' associative deficit originated from high false alarm rates in the associative test. Older adults' high false alarm rates potentially reflect their reduced ability to recollect the study-phase name-face pairs in the presence of intact familiarity with individual names and faces.     

Dissociable contributions within the medial temporal lobe to encoding of object-location associations

The crucial role of the medial temporal lobe (MTL) in episodic memory is well established. Although there is little doubt that its anatomical subregions-the hippocampus, peri-, entorhinal and parahippocampal cortex (PHC)-contribute differentially to mnemonic processes, their specific functions in episodic memory are under debate. Data from animal, human lesion, and neuroimaging studies suggest somewhat contradictory perspectives on this functional specialization: a general participation in declarative memory, an exclusive involvement in associative mnemonic processes, and a specific contribution to spatial memory are reported for the hippocampus, adjacent cortices, and the PHC. A functional lateralization in humans dependent on the verbalizability of the material is also discussed herein. To further elucidate the differential contributions of the various MTL subregions to encoding, we employed an object-location association memory paradigm. The memory for each of the studied associations was tested twice: by the object, and by the location serving as retrieval cue. The memory accuracy in response to both cue types was also assessed parametrically. Brain activity during encoding which leads to different degrees of subsequent memory accuracy under the two retrieval conditions was compared. We found the bilateral posterior PHC to participate in encoding of both the object associated with a location and the location associated with an object. In contrast, activity in an area in the left anterior PHC and the right anterior MTL was only correlated with the memory for the location associated with an object.     

The effects of divided attention at encoding on item and associative memory

Divided attention at encoding is well known to have adverse effects on episodic memory performance (e.g., Naveh-Benjamin & Greg, 2000). This article attempts to determine whether these effects are a result of the interruption of encoding of associative information among the components of an episode. Five experiments, using different types of episodes and episodes components, were conducted. Participants studied information under either full or divided attention and were then tested on their memory for both the episodes' components and the associations between them. Divided attention did not produce a differential deficit in memory for associative information; memory for the components suffered to the same degree as memory for the associations among the components. The cause of the divided-attention effect at encoding lies somewhere other than in the associative processes that are engaged.     

Recognition Memory in Pigeons for Stimuli Presented Repeatedly: Perceptual Learning or Reduced Associative Interference?

Todd and Mackintosh (1990) found that recognition memory of pigeons for pictures was better when the same pictures were used each session (a recency task) than when different slides were used (a novelty task); they attributed the superior performance on the recency task to perceptual learning. Three experiments explored two alternative accounts. One was that their use of a within-subject design could have allowed the strategy adopted in the recency task to influence adversely the strategy used in the novelty task. This possibility was ruled out by Experiment 1, which showed superior performance in the recency task when a between-subject design was used. A second account proposes that slide-reward associations formed (in both tasks) during first presentations of slides interfere with appropriate performance during second presentations (associative interference); in the recency task, however, the high long-term associative strength of the slides restricts the consequence of a single slide-reward pairing to a short-term effect, and associative interference occurs at short retention intervals only. This account was explored in Experiment 2, which found no evidence that increases in retention interval resulted in reduction of associative interference in the recency task, and in Experiment 3, where associative interference was shown to occur but was of comparable magnitude in the recency and novelty tasks. By elimination, the results support a perceptual learning interpretation.     

Memory for age-face associations in younger and older adults: the role of generation and schematic support

Memory for ages of unfamiliar faces was examined in an associative memory task to determine whether generation as well as schematic support (cues from faces) would enhance later cued recall of the age information and reduce older adults' associative deficit. Participants studied faces and were either presented with the age or first had to guess before being shown the correct age. Later, participants were given a cued-recall test. Both younger and older adults exhibited associative memory enhancements from first generating the ages at encoding (a generation effect) despite the fact the initial generation was often inaccurate. Although older adults recalled fewer ages overall compared with younger adults, older adults were able to remember the age information for older faces equally as well as younger adults. However, when errors committed during generation were large and when schematic support was not available to support encoding and retrieval (when the age information was inconsistent given the cues from the face), generating was no longer beneficial for either older or younger adults. Thus, although older adults display an associative deficit when remembering specific age-face associations, this can be reduced through the use of prior knowledge and generation at encoding.     

Episodic encoding and recognition of pictures and words: role of the human medial temporal lobes

In the present PET study, we examined brain activity related to processing of pictures and printed words in episodic memory. Our goal was to determine how the perceptual format of objects (verbal versus pictorial) is reflected in the neural organization of episodic memory for common objects. We investigated this issue in relation to encoding and recognition with a particular focus on medial temporal-lobe (MTL) structures. At encoding, participants saw pictures of objects or their written names and were asked to make semantic judgments. At recognition, participants made yes-no recognition judgments in four different conditions. In two conditions, target items were pictures of objects; these objects had originally been encoded either in picture or in word format. In two other conditions, target items were words; they also denoted objects originally encoded either as pictures or as words. Our data show that right MTL structures are differentially involved in picture processing during encoding and recognition. A posterior MTL region showed higher activation in response to the presentation of pictures than of words across all conditions. During encoding, this region may be involved in setting up a representation of the perceptual information that comprises the picture. At recognition, it may play a role in guiding retrieval processes based on the perceptual input, i.e. the retrieval cue. Another more anterior right MTL region was found to be differentially involved in recognition of objects that had been encoded as pictures, irrespective of whether the retrieval cue provided was pictorial or verbal in nature; this region may be involved in accessing stored pictorial representations. Our results suggest that left MTL structures contribute to picture processing only during encoding. Some regions in the left MTL showed an involvement in semantic encoding that was picture specific; others showed a task-specific involvement across pictures and words. Together, our results provide evidence that the involvement of some but not all MTL regions in episodic encoding and recognition is format specific.     

Speaking of pain in Greek: Implications for the cognitive permeation of emotions

ABSTRACT

Although item-memory for emotional information is enhanced, memory for associations between items is often impaired for negative, emotionally arousing compared to neutral information. We tested two possible mechanisms underlying this impairment, using picture pairs: 1) higher confidence in one’s own ability to memorise negative information may cause participants to under-study negative pairs; 2) better interactive imagery for neutral pairs could facilitate associative memory for neutral pairs more than for negative pairs. Tested with associative recognition, we replicated the impairment of associative memory for negative pairs. We also replicated the result that confidence in future memory (judgments of learning) was higher for negative than neutral pairs. Inflated confidence could not explain the impairment of associative recognition memory: Judgements of learning were positively correlated with associative memory success for both negative and neutral pairs. However, neutral pairs were rated higher in their conduciveness to interactive imagery than negative pairs, and this difference in interactive imagery showed a robust relationship to the associative memory difference. Thus, associative memory reductions for negative information are not due to differences in encoding effort. Instead, interactive imagery may be less effective for encoding of negative than neutral pairs.     

Paying attention to binding: Further studies assessing the role of reduced attentional resources in the associative deficit of older adults

The present experiments investigated whether the observed associative deficit in older adults' episodic memory is mediated by a reduction of attentional resources. Using a dual-task procedure, younger and older participants studied lists of word pairs either under full attention or while performing a concurrent task. Both experiments showed that dividing attention did not cause a greater impairment to memory for associations than to memory for items in either age group. Furthermore, an analysis of concurrent task performance revealed that older adults' attentional costs for both learning and binding items were not larger than for learning items alone, relative to younger adults. These data provide support for a multicausal interpretation of older adults' memory deficits in which common, depleted attentional resources may be a mechanism that reduces memory for components of an episode in both older and younger adults under divided attention at encoding. In addition, older adults have a unique deficit in memory for the associations between the components, which does not seem to be resource dependent.     

The differential effects of emotional salience on direct associative and relational memory during a nap

Relational memories are formed from shared components between directly learned memory associations, flexibly linking learned information to better inform future judgments. Sleep has been found to facilitate both direct associative and relational memories. However, the impact of incorporating emotionally salient information into learned material and the interaction of emotional salience and sleep in facilitating both types of memory is unknown. Participants encoded two sets of picture pairs, with either emotionally negative or neutral objects paired with neutral faces. The same objects were present in both sets, paired with two different faces across the sets. Baseline memory for these directly paired associates was tested immediately after encoding, followed by either a 90-min nap opportunity or wakefulness. Five hours after learning, a surprise test assessed relational memory, the indirect association between two faces paired with the same object during encoding, followed by a retest of direct associative memory. Overall, negative information was remembered better than neutral for directly learned pairs. A nap facilitated both preservation of direct associative memories and formation of relational memories, compared to remaining awake. Interestingly, however, this sleep benefit was observed specifically for neutral directly paired associates, while both neutral and negative relational associations benefitted from a nap. Finally, REM sleep played opposing roles in neutral direct and relational associative memory formation, with more REM sleep leading to forgetting of direct associations but promoting relational associations, suggesting that, while not benefitting memory consolidation for directly learned details, REM sleep may foster the memory reorganization needed for relational memory.     

Implementation intention encoding does not automatize prospective memory responding

An implementation intention encoding, one that specifies the concrete situation that is appropriate for initiating an intended action and links that situational cue to the intended action, has been shown to improve prospective memory. One proposed mechanism is that implementation intentions create automatized prospective remembering. This view anticipates that implementation intentions should prevent prospective memory decline in highly cognitively demanding situations. Contrary to this expectation, although implementation intention encoding enhanced prospective memory (Experiments 1 and 2), implementation-intention encoding did not buffer against significant prospective memory decline in high-cognitive-demand conditions (Experiments 1–3), and in Experiment 3, implementation intention encoding produced lower levels of prospective memory performance than did behavioral practice in the high-cognitive-demand situation. We suggest that although implementation intentions may stimulate a strong associative encoding (between an anticipated environmental cue and an intended action), that encoding does not support a completely automatized prospective memory response.